International Journal of Infectious Diseases 84 (2019) 1–4

Contents lists available at ScienceDirect

International Journal of Infectious Diseases

jo u rn al home pag e: w w w . e l s e v i e r . c o m / l o c a t e / ij id

Management of acute-stage chikungunya disease: Contribution

of ultrasonographic joint examination
Marie Bletterya, Lauren Bruniera, Rishika Banydeenb, Christian Derancourtb,
Michel de Bandta,*
a
Unit of Rheumatology, University Hospital Fort-de-France, Centre Hospitalier de Martinique (CHUM), route de Chateauboeuf, 97200 Fort-de-France, France
b
Unit of Epidemiology and Biostatistics (USMR), Centre Hospitalier de Martinique (CHUM), route de Chateauboeuf, 97200 Fort-de-France, France

ARTICLEINFO
ABSTRACT
Article history:
Received 27 September 2018 Objective: Chikungunya (CHIKV) is an arbovirus that causes acute, debilitating polyarthritis. Its
Received in revised form 21 March 2019 diagnosis can be difficult for clinicians not used to managing joint diseases or detecting synovitis. Joint
Accepted 23 March 2019 Doppler ultrasonography (DUS) is a simple, non-invasive examination, able to visualize synovitis. Its
Corresponding Editor: Eskild Petersen, Aar- diagnostic and prognostic value in rheumatoid arthritis is well-established.
hus, Denmark Methods: Patients with serologically proven acute arbovirosis where included. Clinical examination and
joint count were performed (DAS score). Ultrasound examination was performed by another clinician
Keywords: — experienced in joint DUS — who also performed ultrasound joint score. Joints were examined by
Joint doppler ultrasonography (DUS)
DUS in B-mode looking for: subcutaneous infiltration, effusion, tenosynovitis, erosion and Doppler
Chikungunya
signal.
Viral arthritis
Results: In our experience, joint DUS is able to detect effusions in 92.8% of painful joints, with 28.3% of
the effusions emitting a high-power Doppler signal. No erosion was observed. Subcutaneous
inflammatory infiltration of the ankles (aseptic cellulitis) was found in 28.6% of patients.
Conclusion: Joint DUS is able to detect objective signs responsible for joint pain, which can be useful for
practitioners not accustomed to this type of pathology. It also makes possible distinction between
articular and periarticular manifestations.
© 2019 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).

Introduction
synovial thickening, tenosynovitis and erosions in patients with
persistent pain >1 month after the acute phase, but no
Management of chikungunya virus (CHIKV)-related rheumatic
ultrasound data are available for the early stage of the CHIKV
disease is complex, as previously reported during the Caribbean
disease. During chikungunya there are only ultrasound analyses
outbreak from December 2013 to January 2015 (Marks and Marks,
in secondary and tertiary forms (Manimunda et al., 2010; Moga
2016; Blettery et al., 2016). French recommendations (Simon et al.,
et al., 2018; Canella, 2017; Mogami et al., 2017).
2015) help clinicians in daily practice, because careful recording of
Joint DUS can be a useful tool for clinicians who are not very
patients’ medical histories and serological verification prevent
familiar with joint diseases or not used to detecting synovitis,
errors inherent to the epidemic context and ensure early
can help to make a better clinical evaluation of the articular
therapeutic intervention for these patients. But those
symptoms, could help to differentiate with other arboviruses,
recommendations do not include early examination with joint
and may predict the late articular evolution of the disease.
Doppler ultrasonography (DUS). Although the contribution of
By analogy with rheumatoid arthritis, we hypothesized that
joint DUS to early rheumatoid arthritis diagnosis has been
DUS could be relevant to the evaluation of CHIKV-disease joint
shown (Xiao et al., 2014), joint imaging studies on CHIKV-
and periarticular manifestations. The Echochick Study was part
infected subjects are rare, except (Manimunda et al., 2010; Moga
of the work launched by the University Hospital of Martinique
et al., 2018; Canella, 2017; Mogami et al., 2017). Joint DUS can
(CHUM) at the beginning of the Chikungunya epidemic in 2014.
confirm the presence of joint effusion, bone edema,
The aim of this preliminary study was to determine whether joint
DUS imaging was ofclinicalinterestattheveryearly phaseof CHIKV
disease, to confirm the presence or not of arthritis, to help in the
* Corresponding author at: Unit of Rheumatology, CHU de Martinique, route de positive diagnosis of acute arthritis of Chikungunya and to help
Chateauboeuf, 97200 Fort-de-France, Martinique, France.
in the differential diagnosis with other arboviroses capable of
E-mail address: micheldebandt@gmail.com (M. de Bandt).
causing joint pain.

https://doi.org/10.1016/j.ijid.2019.03.031
1201-9712/© 2019 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2 M. Blettery et al. / International Journal of Infectious Diseases 84 (2019) 1–4

Methods
was confirmed serologically or by polymerase chain reaction
(PCR) (PCR between days 1 and 5, PCR and serology between
Patients (>18 years old) consulting at the CHUM in the
days 5 and 7, and serology alone after day 7). Exclusion criteria
“crisis unit” organized at the beginning of the epidemic in
were: history of chronic inflammatory rheumatic disease, oral
Martinique for acute arthralgias and/or arthritis of <10 days
intake of nonsteroi- dal anti-inflammatory drugs or
duration and possibly related to CHIKV infection were
corticosteroids, lack of demonstra- tion of acute CHIKV
included. Acute CHIKV infection
infection.

Figure 1. Doppler ultrasound examination of a left wrist. Presence of synovitis, with effusion and positive Doppler effect (grade 2, Szkudlarek ’ classification).
 M. Blettery et al. / International Journal of Infectious Diseases 84 (2019) 1–4
Demographic data and physical examination findings were
recorded. The joint count (according to DAS 28) was performed
by the clinician who managed the patient using the same
manage- ment method as in rheumatoid arthritis.
Ultrasound examination was then performed by another
clinician who also performed an ultrasound joint score. Joint
imaging was performed by a senior rheumatologist experienced
in joint DUS (LB). Hands, wrists, feet and ankles were
systematically examined, for the other joints, the 3 most painful
and/or swollen joints were examined and if abnormal findings
were observed, the contralateral joint was systematically
examined. Joints were examined by DUS in B-mode looking for
5 items: subcutaneous infiltration, effusion, tenosynovitis,
erosion and Doppler signal.
Ethics statements
The study was approved by a regional French Ethic
Committee (“Comité de Protection des Personnes, Sud-Ouest et
Outremer III” ; CCP number : 2014/50, ref : 2014-A00875-42).
Written informed consent was obtained from all patients. No
child was included in the study. All patients were adults.
Results
Twenty-eight patients with documented acute CHIKV infection
were enrolled: 19 women and 9 men, mean age 50.7±6 years, and
we also examined 3 patients with acute dengue fever (2 women,
mean age 47± 3). The mean duration of the disease at inclusion
was
5 ± 1 days after clinical onset of manifestations. Acute
Chikungunya was defined by a positive Blood PCR or presence
of IgM antibodies alone and the lack of positivity for dengue
and zika reactions. Acute dengue infection was diagnosed with
negative test for Chikungunya or Zika and positive RT PCR for
Dengue or positive IgM antibodies.
Figure 2. Doppler ultrasound examination of a second MCP. Presence of synovitis, with effusion and positive Doppler effect (grade 1, Szkudlarek ’ classification).
3
For patients with Chikungunya, the average joint count
performed by the clinician was 8 ± 4 painful joints and 4.1± 3
swollen joints. The ultrasound joint score was identical for the
number of painful joints but higher for the number of swollen
joints (7.5 ±2, p 0.02). For patients with dengue fever, the average
number of painful joints was 3, none was swollen either
clinically or by DUS examination.
In CHIKV patients, doppler ultrasonography of painful joints
revealed: effusions in 92.8% of examined joints (75% of hands and
wrists, 50% of ankles, and 35.7% of knees were involved, but
shoulders and elbows were rarely affected). The majority (75.5%) of
effusions detected were unilateral (Figures 1 and 2). We also noted
that not all painful joints are synovitis or effusion sites. A high-
power Doppler signal (grade 2 or 3, Szkudlarek classification) was
emitted by 28.3% of the effusions. Only 2 patients, one with
unilateral and the other bilateral involvement, had detectable
tenosynovitis, this is quite opposite to what is observed in the
chronic phase of chikungunya (Canella, 2017; Mogami et al., 2017).
No erosion was observed. Subcutaneous inflammatory infiltra-
tion (cellulitis) was seen in 13/56 (23.2%) ankles and 8/28 (28.6%)
of
the patients: unilateral in 3 of them and bilateral in 5 (Table 1).
The typical ultrasonographic pattern observed in acute CHIKV
disease was subcutaneous ankle infiltration with asymmetric
arthritis and a positive Doppler signal in one-third of the patients.
During the study period 3 patients with acute dengue fever were
examined by ultrasound and none showed ultrasound joint effusion.
Discussion
The interest of joint ultrasound in the chronic phases of
Chikungunya has been demonstrated in several studies (Moga
et al., 2018; Canella, 2017; Mogami et al., 2017), allowing an
exhaustive joint, periarticular and tendon assessment. No
studies
4 M. Blettery et al. / International Journal of Infectious Diseases 84 (2019) 1–4

Table 1
Joint and periarticular Doppler ultrasonography (DUS) findings in 28 patients during the acute phase of Chikungunya disease.

Joint Subcutaneous infiltration Effusion Tenosynovitis

Unilateral Bilateral Unilateral Bilateral Unilateral Bilateral

No DUS DUS No DUS DUS No DUS DUS No DUS DUS

Shoulder 0 0 0 0 0 0 0 0 0 0
Elbow 0 0 0 1 0 0 0 0 0 0
Wrist 0 0 4 3 3 1 0 1 0 0
Hands (MCP, PIP, DIP) 0 0 6 2 0 2 0 0 0 0
Hip 0 0 2 0 0 0 0 0 0 0
Knee 0 0 7 0 3 0 0 0 0 0
Ankle 3 5 6 4 4 0 0 0 2 0
Foot (MTP) 1 0 3 2 0 0 0 0 0 0

Abbreviations: No DUS, no Doppler effect, hence less aggressive involvement; MCP, metacarpophalangeal; PIP, proximal interphalangeal; DIP, distal interphalangeal; MTP,
metatarsophalangeal.
Values are the numbers of joints affected.

had looked at this exploratory technique in the acute phase of

consent was obtained from all patients. No child was included in
infection.
the study. All patients were adult.
However this kind of work is difficult to perform outside an
epidemic phase, as it has also been difficult to analyze patients
Conflict of interest statement
with another arboviroses over the same period. All patients were
referred in the acute phase of their condition for suspected
None of the authors has any financial and/or personal
arboviroses, which was confirmed in all cases.
relationships with other people or organisations that could
Clearly the ultrasound examination makes the diagnosis
inappropriately influence (bias) their work. Examples of potential
more often than the clinician and detects more manifestations
conflicts of interest include employment, consultancies, stock
than the clinician (who was a rheumatologist trained in clinical
ownership, honoraria, paid expert testimony, patent applications/
joint analysis).
registrations, and grants or other funding.
In our experience, joint DUS enables detection of objective
Nothing to disclose for any author.
signs explaining joint pain, which can be useful for practitioners
No conflict of interest.
not accustomed to dealing with this type of pathology in an
epidemic context or otherwise. It also makes possible distinction
Funding source
between joint and periarticular pathologies.
Despite the very small number of dengue patients in this
No funding source, this is an academic work.
study it seems that joint ultrasound could also differentiate early
between Dengue and Chikungunya, but this must be confirmed
Acknowledgement
on a large scale.
Acute “aseptic ankle cellulitis” is an uncommon clinical sign,
We thank Ms. Janet Jacobson for the proofreading and layout of
usually observed in sarcoidosis (Fernandez-Faith and
this work.
McDonnell, 2007). The presence of (ultrasonographic or clinical)
ankle cellulitis, identical to that seen in acute forms of
References
sarcoidosis, has not been described previously in chikungunya
disease and could be a useful sign to diagnose it. Blettery M, Brunier L, Polomat K, Moinet F, Deligny C, Arfi S, et al. Brief report:
In this study too many patients were lost to follow-up and it management of chronic post-chikungunya rheumatic disease: the Martinican
was not possible to establish a correlation between the initial experience. Arthritis Rheumatol 2016;68(11):2817–24.
Canella C. Imaging in chikungunya fever. Radiol Bras 2017;50(2) V.
joint manifestations and the possible evolution to a chronic Fernandez-Faith E, McDonnell J. Cutaneous sarcoidosis: differential diagnosis. Clin
form. Long- term follow-up of these patients in future Dermatol 2007;25:276–87.
prospective studies will reveal whether the early presence of Manimunda SP, Vijayachari P, Uppoor R, Sugunan AP, Singh SS, et al. Clinical
progression of chikungunya fever during acute and chronic arthritic stages
numerous marked synovitises (with Doppler effect) corresponds
and the changes in joint morphology as revealed by imaging. Trans R Soc
to a chronic course and, therefore, justifies early therapeutic Trop Med Hyg 2010;104(6):392–9.
intervention. Marks M, Marks J. Viral arthritis. Clin Med (Lond) 2016;16(2):129–34.
Moga iR, Vas JLP, Chagas Y, de Abreu M, Sperling-Torezani R, et al.
This preliminary study of ultrasound in the acute phase of an
Ultrasonography of hands and wrists in the diagnosis of complications of
arbovirosis brings elements in favour of the generalization of chikungunya fever. J Ultrasound Med 2018;37(2):511–20.
this approach. Mogami R, Vaz JLP, Chagas YFB, Torezani RS, Vieira AA, et al. Ultrasound of
ankles in the diagnosis of complications of chikungunya fever. Radiol Bras
2017;50 (2):71–5.
Ethics statements Simon F, Javelle E, Cabie A, Bouquillard E, Troisgros O, Gentile G, et al. French
guidelines for the management of chikungunya (acute and persistent
The study was approved by a regional French Ethic presentations). Méd Mal Infect 2015;45:243–63.
Xiao H, Liu M, Tan L, Liao X, Li Y, Gao J, et al. Value of ultrasonography for diagnosis of
Committee (“Comité de Protection des Personnes, Sud-Ouest et synovitis associated with rheumatoid arthritis. Int J Rheum Dis 2014;17(7):767–75.
Outremer III” ; CCP number : 2014/50, ref : 2014-A00875-42).
Written informed